Tri-dimensional and triphasic muscle organization of whole-body pointing movements

Previous kinematic and kinetic studies revealed that, when accomplishing a whole-body pointing task beyond arm's length, a modular and flexible organization could represent a robust solution to control simultaneously target pointing and equilibrium maintenance. Here, we investigated the underlying mechanisms that produce such a coordinative kinematic structure. We monitored the activity of a large number of muscles spread throughout subjects' bodies while they performed pointing movements beyond arm's length, either with or without imposition of postural or pointing constraints. Analyses revealed that muscle signals lied on a tri-dimensional hyper-plane and were temporally organized according to a triphasic pattern (three components, each one exhibiting one single peak of activation and the peaks being consecutive in time). Such a functional muscle synergy was found to be robust across conditions. Also the activities of the separate groups of muscles acting at each body joint resulted tri-dimensional. In particular, those associated with the muscles of the lower-body joints (ankle, knee and hip) always presented the three sequences in all conditions. However, a slightly different organization was found for the muscle activities of the upper-limb, suggesting a moderate level of flexibility of the activity of such muscles to movement constraints. The present findings link together, in a hierarchical view of motor control, the joint coordination characterizing whole-body pointing movements with a basic muscle synergistic organization, namely a triphasic pattern.

[1]  Francesco Lacquaniti,et al.  Modulation of phasic and tonic muscle synergies with reaching direction and speed. , 2008, Journal of neurophysiology.

[2]  G. Cheron,et al.  Does the coordination between posture and movement during human whole-body reaching ensure center of mass stabilization? , 1999, Experimental Brain Research.

[3]  S. Grillner Neurobiological bases of rhythmic motor acts in vertebrates. , 1985, Science.

[4]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[5]  H. Sebastian Seung,et al.  Learning the parts of objects by non-negative matrix factorization , 1999, Nature.

[6]  B. Freriks,et al.  Development of recommendations for SEMG sensors and sensor placement procedures. , 2000, Journal of electromyography and kinesiology : official journal of the International Society of Electrophysiological Kinesiology.

[7]  E. Bizzi,et al.  Muscle synergies encoded within the spinal cord: evidence from focal intraspinal NMDA iontophoresis in the frog. , 2001, Journal of neurophysiology.

[8]  P. Crenna,et al.  A motor programme for the initiation of forward‐oriented movements in humans. , 1991, The Journal of physiology.

[9]  Andrea d'Avella,et al.  Matrix factorization algorithms for the identification of muscle synergies: evaluation on simulated and experimental data sets. , 2006, Journal of neurophysiology.

[10]  David A. Winter,et al.  Biomechanics and Motor Control of Human Movement , 1990 .

[11]  Julia A Leonard,et al.  Reaching to multiple targets when standing: the spatial organization of feedforward postural adjustments. , 2009, Journal of neurophysiology.

[12]  F. A. Mussa-lvaldi,et al.  Convergent force fields organized in the frog's spinal cord , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  Trevor Drew,et al.  Independent and convergent signals from the pontomedullary reticular formation contribute to the control of posture and movement during reaching in the cat. , 2004, Journal of neurophysiology.

[14]  Richard M. Murray,et al.  A Mathematical Introduction to Robotic Manipulation , 1994 .

[15]  Francesco Lacquaniti,et al.  Control of Fast-Reaching Movements by Muscle Synergy Combinations , 2006, The Journal of Neuroscience.

[16]  F. Lacquaniti,et al.  Motor Patterns in Walking. , 1999, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[17]  G. Karst,et al.  Timing of muscle activity during reaching while standing: systematic changes with target distance. , 2004, Gait & posture.

[18]  Wynne A. Lee,et al.  Neuromotor synergies as a basis for coordinated intentional action. , 1984, Journal of motor behavior.

[19]  T. Kaminski The coupling between upper and lower extremity synergies during whole body reaching. , 2007, Gait & posture.

[20]  E. Bizzi,et al.  Stability of muscle synergies for voluntary actions after cortical stroke in humans , 2009, Proceedings of the National Academy of Sciences.

[21]  Torrence D. J. Welch,et al.  A feedback model reproduces muscle activity during human postural responses to support-surface translations. , 2008, Journal of neurophysiology.

[22]  F. P. Kendall,et al.  Muscles: Testing and Function, with Posture and Pain , 1993 .

[23]  E. Bizzi,et al.  Article history: , 2005 .

[24]  Emanuel Todorov,et al.  From task parameters to motor synergies: A hierarchical framework for approximately optimal control of redundant manipulators , 2005, J. Field Robotics.

[25]  Shinji Kakei,et al.  Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons. , 2004, Progress in brain research.

[26]  M. Hallett,et al.  Single-joint rapid arm movements in normal subjects and in patients with motor disorders. , 1996, Brain : a journal of neurology.

[27]  Ryoichi Hayashi,et al.  Afferent feedback in the triphasic EMG pattern of leg muscles associated with rapid body sway , 1998, Experimental Brain Research.

[28]  M. Hallett,et al.  Postural adjustments associated with rapid voluntary arm movements 1. Electromyographic data. , 1984, Journal of neurology, neurosurgery, and psychiatry.

[29]  E. Bizzi,et al.  Central and Sensory Contributions to the Activation and Organization of Muscle Synergies during Natural Motor Behaviors , 2005, The Journal of Neuroscience.

[30]  L. Ferré Selection of components in principal component analysis: a comparison of methods , 1995 .

[31]  R N Lemon,et al.  A novel algorithm to remove electrical cross‐talk between surface EMG recordings and its application to the measurement of short‐term synchronisation in humans , 2002, The Journal of physiology.

[32]  M. D. Neilson,et al.  Motor maps and synergies. , 2005, Human movement science.

[33]  G. Gottlieb,et al.  Coordinating movement at two joints: a principle of linear covariance. , 1996, Journal of neurophysiology.

[34]  Lena H Ting,et al.  Muscle synergy organization is robust across a variety of postural perturbations. , 2006, Journal of neurophysiology.

[35]  François Bonnetblanc,et al.  Modular Control of Pointing beyond Arm's Length , 2009, The Journal of Neuroscience.

[36]  M. Latash,et al.  Flexible muscle modes and synergies in challenging whole-body tasks , 2008, Experimental Brain Research.

[37]  M. Latash,et al.  Muscle synergies during shifts of the center of pressure by standing persons , 2003, Experimental Brain Research.

[38]  Ziaul Hasan,et al.  Kinematic and kinetic constraints on arm, trunk, and leg segments in target-reaching movements. , 2005, Journal of neurophysiology.

[39]  Paul J. Stapley,et al.  Coordination between equilibrium and hand trajectories during whole body pointing movements , 2002, Experimental Brain Research.

[40]  J. Massion,et al.  Forward and backward axial synergies in man , 2004, Experimental Brain Research.

[41]  Emanuel Todorov,et al.  From task parameters to motor synergies: A hierarchical framework for approximately optimal control of redundant manipulators , 2005 .

[42]  D. Humphrey,et al.  Motor control : concepts and issues , 1991 .

[43]  Y. Shinoda,et al.  Innervation of multiple neck motor nuclei by single reticulospinal tract axons receiving tectal input in the upper cervical spinal cord , 1994, Neuroscience Letters.

[44]  F. Lacquaniti,et al.  Coordination of Locomotion with Voluntary Movements in Humans , 2005, The Journal of Neuroscience.

[45]  T. Pozzo,et al.  Evidence of a preprogrammed deactivation of the hamstring muscles for triggering rapid changes of posture in humans. , 1997, Electroencephalography and clinical neurophysiology.

[46]  F. Lacquaniti,et al.  Five basic muscle activation patterns account for muscle activity during human locomotion , 2004, The Journal of physiology.